Overlapping Features of Primary Cutaneous Marginal Zone Lymphoproliferative Disorder and Primary Cutaneous CD4 + Small/Medium T-Cell Lymphoproliferative Disorder : A Diagnostic Challenge Examined by Genomic Analysis.
Journal
The American journal of surgical pathology
ISSN: 1532-0979
Titre abrégé: Am J Surg Pathol
Pays: United States
ID NLM: 7707904
Informations de publication
Date de publication:
01 03 2023
01 03 2023
Historique:
pmc-release:
01
03
2024
pubmed:
5
1
2023
medline:
25
2
2023
entrez:
4
1
2023
Statut:
ppublish
Résumé
Primary cutaneous marginal zone lymphoproliferative disorder (PCMZL) and primary cutaneous CD4 + small/medium T-cell lymphoproliferative disorder (CD4 + TLPD) are indolent lymphoproliferative disorders. However, cases with overlapping features can be challenging. We identified 56 CD4 + TLPD and 38 PCMZL cases from our pathology archives. Clinical, morphologic, and immunophenotypic features were reviewed. Polymerase chain reaction for immunoglobulin (IG) and T-cell receptor gamma (TRG) gene rearrangements were analyzed. Next-generation sequencing studies were performed on 26 cases with adequate material, 19 with CD4 + TLPD, and 7 with PCMZL. CD4 + TLPD presented mostly (91%) as solitary lesions, located in the head and neck area (64%), while PCMZL occurred mostly in the upper extremity (47%) and trunk (34%). Lesions were sometimes multiple (40%) and recurrences (67%) were more common. Cases of PCMZL had an increase in reactive CD3 + T cells, with frequent programmed cell death protein 1 expression, whereas cases of CD4 + TLPD often contained abundant reactive B cells. Twenty-five cases were identified as having overlapping features: 6 cases of PCMZL were clonal for both IG and TRG; 11 cases of CD4 + TLPD were clonal for IG and TRG and 6 cases of CD4 + TLPD had light chain-restricted plasma cells. By next-generation sequencing, 23 variants were detected in 15 genes, with PCMZL more likely to show alterations, most commonly affecting TNFAIP3 and FAS, altered in 5 cases. Both entities have an indolent clinical course with response to conservative therapy and management, and warrant interpretation as a lymphoproliferative disorder rather than overt lymphoma.
Identifiants
pubmed: 36598455
doi: 10.1097/PAS.0000000000001984
pii: 00000478-202303000-00008
pmc: PMC9974535
mid: NIHMS1839241
doi:
Types de publication
Journal Article
Research Support, N.I.H., Intramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
344-353Subventions
Organisme : Intramural NIH HHS
ID : ZIA SC000550
Pays : United States
Informations de copyright
Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.
Déclaration de conflit d'intérêts
Conflicts of Interest and Source of Funding: Supported by the Intramural Research Program of the Center for Cancer Research, National Cancer Institute, National Institutes of Health. The authors have disclosed that they have no significant relationships with, or financial interest in, any commercial companies pertaining to this article.
Références
Willemze R, Cerroni L, Kempf W, et al. The 2018 update of the WHO-EORTC classification for primary cutaneous lymphomas. Blood. 2019;133:1703–1714.
Leinweber B, Beltraminelli H, Kerl H, et al. Solitary small- to medium-sized pleomorphic T-cell nodules of undetermined significance: clinical, histopathological, immunohistochemical and molecular analysis of 26 cases. Dermatology. 2009;219:42–47.
Beltraminelli H, Leinweber B, Kerl H, et al. Primary cutaneous CD4+ small-/medium-sized pleomorphic T-cell lymphoma: a cutaneous nodular proliferation of pleomorphic T lymphocytes of undetermined significance? A study of 136 cases. Am J Dermatopathol. 2009;31:317–322.
Beltzung F, Ortonne N, Pelletier L, et al. Primary cutaneous CD4+ small/medium T-cell lymphoproliferative disorders: a clinical, pathologic, and molecular study of 60 cases presenting with a single lesion: a multicenter study of the French Cutaneous Lymphoma Study Group. Am J Surg Pathol. 2020;44:862–872.
Rodríguez Pinilla SM, Roncador G, Rodríguez-Peralto JL, et al. Primary cutaneous CD4+ small/medium-sized pleomorphic T-cell lymphoma expresses follicular T-cell markers. Am J Surg Pathol. 2009;33:81–90.
Garcia-Herrera A, Colomo L, Camos M, et al. Primary cutaneous small/medium CD4+ T-cell lymphomas: a heterogeneous group of tumors with different clinicopathologic features and outcome. J Clin Oncol. 2008;26:3364–3371.
Grogg KL, Jung S, Erickson LA, et al. Primary cutaneous CD4-positive small/medium-sized pleomorphic T-cell lymphoma: a clonal T-cell lymphoproliferative disorder with indolent behavior. Mod Pathol. 2008;21:708–715.
Swerdlow SH, Campo E, Pileri SA, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood. 2016;127:2375–2390.
Campo E, Jaffe ES, Cook JR, et al. The International Consensus Classification of Mature Lymphoid Neoplasms: a report from the Clinical Advisory Committee. Blood. 2022;140:1229–1253.
Dalle S, Thomas L, Balme B, et al. Primary cutaneous marginal zone lymphoma. Crit Rev Oncol Hematol. 2010;74:156–162.
Edinger JT, Kant JA, Swerdlow SH. Cutaneous marginal zone lymphomas have distinctive features and include 2 subsets. Am J Surg Pathol. 2010;34:1830–1841.
Carlsen ED, Swerdlow SH, Cook JR, et al. Class-switched primary cutaneous marginal zone lymphomas are frequently IgG4-positive and have features distinct from IgM-positive cases. Am J Surg Pathol. 2019;43:1403–1412.
De Souza A, Ferry JA, Burghart DR, et al. IgG4 expression in primary cutaneous marginal zone lymphoma: a multicenter study. Appl Immunohistochem Mol Morphol. 2018;26:462–467.
Çetinözman F, Koens L, Jansen PM, et al. Programmed death-1 expression in cutaneous B-cell lymphoma. J Cutan Pathol. 2014;41:14–21.
Egan C, Laurent C, Alejo JC, et al. Expansion of PD1-positive T cells in nodal marginal zone lymphoma: a potential diagnostic pitfall. Am J Surg Pathol. 2020;44:657–664.
Magro CM, Ruan J, Grossman M, et al. Monoclonal plasma cell infiltrates in the setting of cutaneous follicular helper T cell lymphoproliferative disorders. Ann Diagn Pathol. 2019;40:94–104.
Kazakov DV, Kutzner H, Palmedo G, et al. Primary cutaneous lymphoproliferative disorders with dual lineage rearrangement. Am J Dermatopathol. 2006;28:399–409.
Callan MFC, Steven N, Krausa P, et al. Large clonal expansions of CD8+ T cells in acute infectious mononucleosis. Nat Med. 1996;2:906–911.
Plasilova M, Risitano A, Maciejewski JP. Application of the molecular analysis of the T-cell receptor repertoire in the study of immune-mediated hematologic diseases. Hematology. 2003;8:173–181.
Shi M, Olteanu H, Jevremovic D, et al. T-cell clones of uncertain significance are highly prevalent and show close resemblance to T-cell large granular lymphocytic leukemia. Implications for laboratory diagnostics. Mod Pathol. 2020;33:2046–2057.
Maini MK, Casorati G, Dellabona P, et al. T-cell clonality in immune responses. Immunol Today. 1999;20:262–266.
Stewart JP, Gazdova J, Darzentas N, et al. Validation of the EuroClonality-NGS DNA capture panel as an integrated genomic tool for lymphoproliferative disorders. Blood Adv. 2021;5:3188–3198.
Swerdlow SH, Campo E, Harris NL, et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. International Agency for Research on Cancer (IARC); 2017.
Jaffe ES. Navigating the cutaneous B-cell lymphomas: avoiding the rocky shoals. Mod Pathol. 2020;33:96–106.
Colli C, Leinweber B, Mullegger R, et al. Borrelia burgdorferi-associated lymphocytoma cutis: clinicopathologic, immunophenotypic, and molecular study of 106 cases. J Cutan Pathol. 2004;31:232–240.
Cho-Vega JH, Vega F, Rassidakis G, et al. Primary cutaneous marginal zone B-cell lymphoma. Am J Clin Pathol. 2006;125(suppl:):S38–S49.
Jung H, Yoo HY, Lee SH, et al. The mutational landscape of ocular marginal zone lymphoma identifies frequent alterations in TNFAIP3 followed by mutations in TBL1XR1 and CREBBP. Oncotarget. 2017;8:17038–17049.
Vela V, Juskevicius D, Gerlach MM, et al. High throughput sequencing reveals high specificity of TNFAIP3 mutations in ocular adnexal marginal zone B-cell lymphomas. Hematol Oncol. 2020;38:284–292.
Schmitz R, Hansmann ML, Bohle V, et al. TNFAIP3 (A20) is a tumor suppressor gene in Hodgkin lymphoma and primary mediastinal B cell lymphoma. J Exp Med. 2009;206:981–989.
Maurus K, Appenzeller S, Roth S, et al. Panel sequencing shows recurrent genetic FAS alterations in primary cutaneous marginal zone lymphoma. J Invest Dermatol. 2018;138:1573–1581.
Fisher GH, Rosenberg FJ, Straus SE, et al. Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell. 1995;81:935–946.
Hsu AP, Dowdell KC, Davis J, et al. Autoimmune lymphoproliferative syndrome due to FAS mutations outside the signal-transducing death domain: molecular mechanisms and clinical penetrance. Genet Med. 2012;14:81–89.
Streubel B, Vinatzer U, Lamprecht A, et al. T(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma. Leukemia. 2005;19:652–658.
Murga Penas EM, Hinz K, Röser K, et al. Translocations t(11;18)(q21;q21) and t(14;18)(q32;q21) are the main chromosomal abnormalities involving MLT/MALT1 in MALT lymphomas. Leukemia. 2003;17:2225–2229.
Wongchaowart NT, Kim B, Hsi ED, et al. t(14;18)(q32;q21) involving IGH and MALT1 is uncommon in cutaneous MALT lymphomas and primary cutaneous diffuse large B-cell lymphomas. J Cutan Pathol. 2006;33:286–292.
Pillonel V, Juskevicius D, Ng CKY, et al. High-throughput sequencing of nodal marginal zone lymphomas identifies recurrent BRAF mutations. Leukemia. 2018;32:2412–2426.
McKinney M, Moffitt AB, Gaulard P, et al. The genetic basis of hepatosplenic T-cell lymphoma. Cancer Discov. 2017;7:369–379.
Tomita S, Kikuti YY, Carreras J, et al. Monomorphic epitheliotropic intestinal T-cell lymphoma in asia frequently shows SETD2 alterations. Cancers. 2020;12:3539.